Seasonality of Old World Screwworm Myiasis in the Mesopotamia Valley in Iraq

Medical and Veterinary Entomology (2005) 19, 140–150

Seasonality of Old World screwworm myiasis in the Mesopotamia valley in Iraq

A. SIDDIG1 , S. AL JOWARY2 , M. AL IZZI3 , J. HOPKINS4 ,M.J.R.HALL5 and J. SLINGENBERGH4 1Ministry of Science and Technology, Khartoum, Sudan, 2College of Education for Women, University of Baghdad, Baghdad, Iraq, 3Entomology Department, Iraqi Atomic Energy Commission, Ministry of Science and Technology, Baghdad, Iraq, 4Animal Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy and 5The Natural History Museum, London, U.K.

Abstract. Following the first recorded introduction of the Old World screwworm fly (OWS), Chrysomya bezziana Villeneuve (Diptera: Calliphoridae), into the Mesopotamia valley in Iraq in September 1996, cases of livestock myiasis caused by OWS developed a distinctly seasonal pattern. The annual cycle of clinical OWS cases is explained here on the basis of environmental variables that affect the different life-cycle stages of C. bezziana. This analysis suggests that low temperatures restricted pupal development during the winter, whereas the dispersal of adult flies was constrained by hot/dry summer conditions. A restricted number of OWS foci persisted throughout the year. In these foci, pupal development was fastest during the autumn months. In autumn, rapid multiplication, lasting several OWS generations, allowed subsequent adult fly dispersal across the valley floor during the winter. Hence, the monthly incidence of clinical OWS cases in livestock peaked during December–January and was lowest during July–August. In addition to temperature and humidity, vegetation cover played a role in OWS distribution. Hence the majority of OWS cases were clustered in the medium density type of vegetation [normalized difference vegetation index (NDVI) values of 0.2–0.4] along the main watercourses in the marshy Mesopotamia valley. Although sheep were the host most commonly infested by C. bezziana, local sheep density was not found to be a major factor in disease spread. Satellite imagery and the application of Geographical Information System (GIS) tools were found to be valuable in understanding the distribution of OWS in relation to vegetation and watercourses. The presence of screwworm in Iraq, at the perimeter of the intercontinental OWS distribution, may give rise to major seasonal flare-ups. Key words. Chrysomya bezziana, geographical information system, myiasis, Old World screwworm, seasonality, sheep, Iraq.

Introduction fly (NWS), Cochliomyia hominivorax Coquerel, have a very similar biology, ecology and behaviour (Spradbery, 1994) Although classified in different genera of the blowfly family, and both species are obligate parasites of vertebrates in Calliphoridae, the Old World screwworm fly (OWS), Chry- their larval stages, causing traumatic myiasis. There is no somya bezziana Villeneuve, and the New World screwworm overlap in their geographical distributions. NWS is confined to the Americas, but OWS is found across sub- Saharan Africa, the Indian subcontinent, South-east Asia, Correspondence: Dr Awatif Siddig, Ministry of Science and and the Gulf region of the Arabian Peninsula (Norris & Technology, Animal Resources Research Corporation, 6 Street no. Murray, 1964). Molecular analysis of OWS populations 1 Al Amarat, Khartoum, Sudan. Tel: +24 99 1269 4430; fax: from sub-Saharan Africa, the Gulf region and Asia suggests 24 91 8347 2690; E-mail: [email protected] that the geographical isolation of the sub-Saharan African

140 # 2005 The Royal Entomological Society Old World screwworm in Iraq 141 and Asian lineages of C. bezziana took place about one More permanent infestations appear to have occurred in million years ago (Hall et al., 2001). This static distribution the Sultanate of Oman and in Iraq. A 10-month survey pattern is surprising given that domestic livestock have carried out in the Sultanate of Oman during 1989–1990 replaced wild ungulates as the most commonly infested found 82 OWS cases in the northern part of the country host animals throughout most of the geographical range during the cooler months of the year (Spradbery et al., of OWS. Livestock numbers across the world are on the 1992). The first introduction of OWS into Iraq reportedly increase and so is the annual trade in live animals (FAO- took place in June 1996 (Abdul Rassoul et al., 1996). STAT, 2001). It may be expected that further spread of Traumatic myiasis assumed epidemic proportions during livestock will occur and, with them, there is the potential the winter months of late 1996 and early 1997 (Hopkins & for spread of parasites and pathogens. Khattat, 1997), ultimately giving rise to 9306 and 45 398 The Middle East region is an area of particular interest, cases in 1996 and 1997, respectively (Al-Adhadh, 2001). with extensive livestock movement. It has been suggested Scarcity of insecticide limited effective disease control and that the isolation of African and Asian OWS lineages is a second epidemic wave developed during the second maintained by the zone of unfavourable arid environments winter, with a monthly incidence amounting to 23 000 between the Gulf and sub-Saharan Africa (Hall et al., 2001). OWS clinical cases in December 1997 (Al-Izzi et al., Even so, it remains unclear why African lineage OWS have 1999a). During 1998, significant quantities of insecticide so far not been detected in the Arabian Peninsula given that became available to the veterinary clinics and the incidence millions of live ruminants are imported every year from the was eventually reduced. The objective of the present study Greater Horn of Africa. Also difficult to explain is the fact was to examine the interaction of environmental factors and that screwworm flies have not become established in fly biology that gave rise to the observed seasonality of Australia, despite the presence of OWS in Papua New OWS myiasis cases. Guinea and the occasional detection of dead C. bezziana flies in light fittings on livestock vessels returning from the Gulf area or on-board commercial aircraft arriving from OWS-infested India (Rajapaksa & Spradbery, 1989). Materials and methods Although the global OWS and NWS picture has remained relatively unchanged, there has been considerable Collection of case data local spread, particularly at the perimeter of the continental OWS and NWS fly distributions. Outbreaks of NWS In September 1996, the presence of OWS in Iraq was myiasis occurred in the United States during the 1930 s, confirmed by the FAO Collaborating Centre on Myiasis reaching Florida and then the south-eastern states in 1933 Causing Insects and their Identification at the Natural His- and extending up to the great lakes in 1935 (Readshaw, tory Museum in London, U.K. (Hall, 1997). Subsequently, 1986). Mild winters and moist summers supported the strict guidelines were issued to field veterinary services and widespread persistence of NWS, until its eradication by clinics on how to record any clinical cases of traumatic the Sterile Insect Technique (SIT) (Wyss, 2001). A shipment myiasis in livestock, detailing host species, breed, age and of NWS-affected livestock is believed to have brought locality for each case encountered. Medical centres received C. hominivorax from the Americas to northern Libya in instructions for the recording of human cases. 1988 (Gabaj et al., 1989; Lindquist et al., 1992). Here also, Field data were collated bimonthly and the findings SIT was applied to eradicate the incursion (FAO, 1992). reported to relevant national, regional and international The success of the SIT campaign was probably enhanced organizations. Clinical cases of traumatic myiasis caused by low winter temperatures in both the Southern United by C. bezziana were identified and recorded by veterinarians States (Readshaw, 1986) and Libya (Krafsur & Lindquist, in a network of 111 government veterinary clinics (Al-Ani, 1996). 1997; Al-Taweel et al., 2000), which were geo-referenced for In 1983, an accidental introduction of C. bezziana from a the production of digital maps. Identifications were based ship reportedly took place in the coastal Salalah area of the on the descriptions given by Zumpt (1965) and Spradbery Sultanate of Oman (Spradbery et al., 1992). A total of (1991) and sub-samples were confirmed by the 10 500 animals became affected until the situation was Natural History Museum in Baghdad. They are believed finally brought in check by insecticide treatments. Similarly, to present an accurate record of OWS cases because C. bezziana spread out from the Gulf port of Booshehr, this species was the only one in the region responsible Iran, in April 1995 (Navidpour et al., 1996; Haddadzadeh for the deeply penetrating wounds characteristic of et al., 1997), prompting a major insecticidal campaign. screwworm species. Wohlfahrtia magnifica (Diptera: Minor incursions have also occurred in other Gulf States, Sarcophagidae), which produces similar wounds, is also including an introduction of C. bezziana into Bahrain in found in Iraq, but only in the northern regions and not 1977 (Kloft et al., 1981) and into the United Arab Emirates in cases reported here. The monthly incidences of OWS in in 1988 (Spradbery & Kirk, 1992). Sporadic cases of OWS livestock considered here were just those recorded for the myiasis also occur in Saudi Arabia, in humans (Ansari & first 2 years following OWS introduction. Subsequently the Oertley, 1982) and livestock (Alahmed, 2002; El-Azazy & use of insecticides increased, distorting natural population El-Metenawy, 2004). levels.

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Collection of Old World screwworm fly biological data 100 mL of water. Dead adults were collected daily and adult life span was calculated as the period from the first day of An OWS fly-rearing unit was established in the Entomology emergence until death. New adult cages were prepared Department of the Iraqi Atomic Energy Commission in 1996, weekly or biweekly and left outside in the same site, always in the Tuwaitha region of south Baghdad. To obtain data on under shade, from September 1998 to August 1999 (Al-Izzi pupal survival of laboratory-reared C. bezziana, a wooden box et al., 1999a,b; Al-Jowary, 2000). Although it is appreciated (35 27 10 cm) was divided into 15 cells (7 9cm)andafine that adult survival outside in cages might not be a realistic metal mesh closed the base. Each cell was filled with moist sand. reflection of the mortality of wild flies, we were interested in Thirty mature larvae, taken from the colony just before pupar- this study in comparative rather than absolute values and our iation, were introduced into the box at a density of two larvae protocol enabled monthly comparisons of longevity to be per cell. Shortly after pupariation, the box was placed outside to made where the only variable was the local climate. expose the pupae to field conditions. The box was left on the soil Climate data were collected from a thermohygrograph surface under the shade of a tree. A glass vial covered each pupa located at the experimental site and also from the Baghdad in order to confine the adult when it emerged. Monthly experi- meteorology station, located 5 km from the site. ments were run, from September 1998 to August 1999. Proto- cols for larval rearing and handling were obtained from Digital mapping Spradbery (1992) and Al-Izzi et al. (1999b). To obtain data on adult survival of laboratory-reared Digitized maps showing monthly OWS distribution, as C. bezziana, for matching against the monthly humidity and co-ordinates of the veterinary clinics and their OWS case temperature conditions, 50–100 pairs of newly emerged data, were taken for further analysis into an ArcView Geo- adults were placed inside cages (either 0.5 0.5 0.5 m or graphical Information System (GIS) environment and 1.5 1.5 2.0 m) made from black or white cloth netting, related to climate data, to information on livestock distri- suspended inside a metal frame (either 0.51 0.51 0.51 m bution and to satellite imagery, which indicated vegetation or 1.52 1.52 2.01m).Fourtosixcageswereusedatany cover, landscape, topography and watercourse distribution. one time, their size depending on the number of adults that Vegetation index information were taken from the monthly emerged, i.e. small cages for 50 pairs of adults and bigger (average of the monthly maximum for years 1998–2001) cages for greater numbers (cage size did not affect adult normalized difference vegetation index (NDVI) values pro- longevity at the fly densities used). To provide natural venti- duced and made available by FAO ARTEMIS at a 1 km2 lation in field conditions, the cages were kept outdoors in the resolution (http://metart.fao.org). These values were shade of a tree. The flies were provided with water and food derived from data from the VEGETATION instruments in a dish containing cotton wool saturated with water, granu- onboard the SPOT-4 polar orbiting satellite, after pro- lated sugar, honey and ground beef. An additional protein cessing the output using the following equation, source was provided, formulated by mixing 50 g of spray- NDVI ¼ (IR R)/(IR þ R), where IR stands for the infra- dried cow blood and 50 g of dry chicken eggs and then red band and R stands for the visible red band. The NDVI transferring 10 g of this mixture to the feeding container in values were categorized into the following zones of

25000

20000

15000

10000

5000 Number of cases of OWS reportedNumber of cases OWS monthly 0 Jul-97 Jul-98 Oct-96 Apr-97 Oct-97 Apr-98 Jan-97 Jun-97 Jan-98 Jun-98 Feb-97 Feb-98 Mar-97 Mar-98 Aug-97 Aug-98 Nov-96 Nov-97 Dec-96 Dec-97 Sep-96 Sep-97 May-97 May-98

Fig. 1. The monthly Old World screwworm fly (OWS) incidence (number of cases recorded at government veterinary clinics) in Iraq for the period September 1996 to August 1998.

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150 Old World screwworm in Iraq 143 vegetation cover: high vegetation (> 0.4), medium vegetation valley during the first full year of establishment of OWS in (0.2–0.4), light vegetation (0.1–0.2), and bare soil (< 0.1). Iraq (Fig. 2). The original foci of OWS cases observed during These arbitrary NDVI categories give a measure of vegeta- the autumn outbreak, September 1996, were in an approxi- tion amount and condition and are representative of plant mately linear distribution around the Tigris river system assimilation condition and of its photosynthetic apparatus (Fig. 2a), with few cases along the Euphrates system. During capacity and biomass concentration (Loveland et al., 1991; the following winter and spring months, there was not only a Groten, 1993). They were not equated here to particular spread of these foci along the Tigris, but also a more signifi- plant taxa. The display and integration of satellite imagery, cant expansion of the range along the Euphrates river system digital maps and associated databases were facilitated by (Fig. 2b). The number of cases of OWS declined during the FAO Windisp4 software (http://metart.fao.org). first summer months, with populations retreating mainly into Euphrates refugia (Fig. 2c). However, these same refugia provided the base for a more pronounced expansion in the Results second winter, indicated by the increase in number and concentration of OWS cases along the Euphrates starting in Seasonality of Old World screwworm fly case numbers and September–October 1997 (Fig. 2d). distribution Seasonality of meteorological conditions and their effect on In both years of the study, the monthly OWS case inci- Old World screwworm fly development dence peaked in the period of late autumn to early winter and declined sharply in springtime, reaching a low during To explain variability in monthly OWS case incidence, in the long, hot and dry summer (Fig. 1). both time and space, the observed seasonal pattern was OWS appeared to disperse along the main rivers and related to relevant environmental variables. In the Baghdad major tributaries of the lower lying areas of the Mesopotamia area there was a considerable contrast between the cool/wet a

Euphrates Iran

Tigris

OWS cases September 96 N

1–3

4–6

7–18 0 20 40 80 Kilometers

Fig. 2. The spatial distribution of Old World screwworm fly (OWS) along the main rivers and major tributaries in the Mesopotamia valley during: (a) first records of introduction of September 1996; (b) population expansion period of October 1996–April 1997; (c) summer refugia period of July–August 1997; and (d) foci for expansion at the start of the second season, September–October 1997.

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Euphrates Iran

Tigris

OWS cases Oct 96_Apr 97

3–46 47–122 N 123–227 228–550 551–1538 0 20 40 80 Kilometers

Fig. 2. Continued. winter (November–February) and the hot/dry summer from large watercourses of all veterinary clinics report- (June–August) (Fig. 3). ing cases of OWS each month during 1996–1997 and the For the laboratory-reared larvae, a positive and significant observed longevity of the laboratory-reared flies each (R2 ¼ 0.988) linear relationship was observed between the month during 1998–1999, together with the average monthly values of average mean daily temperature and rate monthly air temperatures during those two periods. of pupal development (reciprocal of the duration [days] of the Longevity and distance data could not be collected pupal stage) (Fig. 4). Spradbery (1992) established a similar for the same periods; however, these periods were very relationship in the laboratory using climate-controlled cabinets similar in relation to temperature (Fig. 5). Large water- (Fig. 4, dashed line). No flies emerged during July and August courses were defined as the main rivers, their tributaries 1999 when ambient temperatures exceeded 35 C and pupae and canals. Distances of clinics from watercourses died. Pupal development was also low during the low tempera- were measured using Arc View. No new foci became tures of November to March. Adult flies did emerge, but only established during the hot/dry August of 1997, when after an extended pupal development of up to 3–4 weeks and flies suffered from adverse weather conditions. In the only 21–44% of adults emerged. Emergence rates during the same period of 1998, adult longevity was only 5–8 days months of autumn (September–October) and spring (April– (Fig. 5). Inverse relationships were apparent between June) contrasted strongly with rates observed during winter adult longevity and temperature and between average and summer. Hence, pupal development during this period distance from watercourses and temperature. The ranged from 5 to 9 days and 54–77% of flies emerged. effect of these relationships on fly longevity and distribution was such that during the winter period Relationship between major water sources and Old World when adult flies lived longest the average distance screwworm fly distribution from the major water sources was greatest. Hence, the geographical distribution of OWS cases was greatest in The impact of major water sources on OWS distribu- the period when adult fly survival was also greatest and tion was considered by plotting the average distance vice versa.

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Euphrates Iran

Tigris

N OWS cases July_August 97 1–5 6–14 15–21 0 20 40 80 Kilometers 22–89

Fig. 2. Continued.

Relationship between the distributions of vegetation and of areas and OWS presence (y ¼ 5353.4x þ 0.1, R2 ¼0.03, Old World screwworm fly cases d.f. ¼ 16, P < 0.49). In addition, at the resolution of village level, the number of sheep per clinic and corres- The first records of OWS cases at veterinary clinics that ponding OWS incidence per clinic were analysed, but were previously free of OWS were largely reported from no significant correlation was found between them September to January, during both 1996–1997 and (y ¼54.151x þ 64815, R2 ¼ 0.007, d.f. ¼ 109, P ¼ 0.37). 1997–1998. Although individual flies are naturally capable of covering large distances (Spradbery, 1994; Spradbery et al., 1995), OWS cases remained mainly confined to the Discussion medium category vegetation coverage at all times, during both high and low periods of OWS case incidence (Fig. 6). During the last two decades of the 20th century, major This suggests that the extent of colonization of the ecological changes occurred in the southern marshlands of Mesopotamia valley floor under optimal conditions was the Mesopotamia valley due to drainage (Partow, 2001). primarily dictated by the vegetation pattern. However, these marshlands remained uninfested by OWS during the study period and it was concluded that there was no discernible causal relationship between drainage of the Relationship between the distributions of sheep and of Old marshlands and OWS outbreaks. World screwworm fly cases A climate matching model (CLIMEX) indicates that OWS is most successful under hot and wet conditions and The relationship between the distribution of sheep and is sensitive to prolonged cold or dryness (Sutherst et al., the numbers of OWS cases was explored at different levels 1989). Hot and wet conditions are not encountered in Iraq of resolution. At the national level and just using areas and therefore the climate is marginal for OWS develop- covered by vegetation bands 0.2–0.4, there was no statisti- ment. The initial focus of OWS within the Mesopotamia cally significant correlation between major sheep-keeping valley was in the Tigris river system, but the distribution

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Euphrates Iran

Tigris

OWS cases Sept_Oct 97

1–8

9–19 N 20–34

35–58

59–131 0 20 40 80 Kilometers

Fig. 2. Continued. expanded during the first winter period, when conditions class appeared far more important as a determinant of the for adult fly survival were seasonally ideal, following an distribution of OWS cases. The OWS distribution pattern autumn period optimal for pupal development. Although broadly agreed with the amount of medium-dense type of the population declined in the summer of 1997, it had by vegetation along the Tigris and Euphrates rivers and major then become established in the previously OWS-free tributaries. Although it is difficult to accurately depict all Euphrates river system. Hence the second season of expan- areas of potential spread, it appears that most areas with sion was even more pronounced than the first (Fig. 1), with medium-dense vegetation have now become invaded: few the number and distribution of the OWS refugia that OWS cases have been found in open areas of either low enabled summer survival being indicative of the magnitude vegetation, despite the presence of veterinary clinics in those of the following autumn and winter outbreaks. The sea- areas, or dense swamp vegetation. Adult flies avoid the high sonal picture became one of expansion of OWS populations temperatures and high solar radiation encountered in open as marginal habitats became tolerable, followed by contrac- areas of bare soil without any vegetation. The fact that there tion of populations as habitat suitability again declined. were few OWS cases recorded along the greenest, riverine The initial spread of OWS within Iraq was probably vegetation might be explained by the scarcity of livestock enhanced by a shortage of insecticide and by an inadequate on, and consequent placement of veterinary clinics away means to distribute it. from, this irrigated arable land. No relationship was found between sheep populations and As vegetation type appears to be a critical factor in OWS numbers of OWS cases in our study. However, the data on epidemiology, it is relevant to recall the widespread eco- national sheep distribution was not very detailed, and the logical change brought about by the construction of river OWS distribution, determined here by distribution of cases dams upstream of the Tigris and Euphrates rivers in at veterinary clinics, may not have represented the ecological Turkey, Syria and Iraq. As a result of these dams, some limit of OWS spread. Since 1997, OWS has become gradually 20 000 km2 of lake areas within the Mesopotamia valley more widespread in Iraq, albeit within the Mesopotamia dried out. OWS may one day appear in this new environ- valley. Compared to sheep density, the vegetation index ment as it becomes vegetated. OWS could also potentially

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150 Old World screwworm in Iraq 147

70 Wet/Cool 65 Jan 60 Dec Nov 55 Feb 50 Oct 45 Mar Apr 40 Sep

35 Jun May 30 Aug Jul Mean daily relative humidity (RH%) Mean daily relative 25 Dry/Hot 20 12 14 16 18 20 22 24 26 28 30 32 34 36 38 Mean daily temperature (C)

Fig. 3. Monthly average mean temperature and relative humidity for the Baghdad area (Source: Baghdad Climate Station, Meteorological Office of Iraq via Arab Organization for Agriculture Development). spread further along the Euphrates river system, into Syria. lished in irrigated areas with tree cover. These OWS foci It is notable that the veterinary inspection at the Iraq/Syria disappeared when the feedlots were moved to dry locations border was intensified following the detection of an OWS- (Kloft et al., 1981). infected animal there in June 1997, just 12 km from the Although the seasonal expansion and contraction of border with Syria (Spradbery & El-Dessouky, 1998). The OWS populations could be influenced by a range of factors, Mesopotamia valley type of ecology is also found in adja- such as the extent of OWS spread during the previous cent regions of Iran, where Iran has reported OWS pro- month, local vegetation, host abundance and movements blems to occur (Navidpour et al., 1996; Haddadzadeh et al., of infested animals, the data suggest (Fig. 5) that the hot/ 1997). OWS was reported from Kuwait in 1997 and 1998 dry summer conditions (June–August) are least favourable (source: routine reports of OWS Coordinator to FAO), but for adult fly survival and population spread. has since been eradicated by chemical means. Infestations in Although the areas affected by OWS within the Arabian Bahrain were only supported when feedlots were estab- Peninsula may remain restricted, OWS is capable of increasing

0.2 Jun99 0.18 May99 0.16 Sep98 0.14 Oct98 0.12 Apr99

0.1

0.08 Mar99 0.06

Pupal development rate (1/days) rate Pupal development Nov98 Feb99 0.04 Jan99 Dec98 0.02 12 14 16 18 20 22 24 26 28 30 32

Mean daily temperature (C)

Fig. 4. The relationship between temperature and duration of Old World screwworm fly (OWS) pupal development (1/no. of days), from Spradbery (1992; shown as a dashed line) and that observed under field conditions in Iraq from September 1998 to June 1999 (shown as monthly squares, regression line not fitted, y ¼ 0.0079x 0.0679, R2 ¼ 0.977).

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50 40

35 40 30

30 25

20 20 Temperature (C) Temperature 15 10 10

0 5 JUL JAN JUN FEB SEP APR MAY OCT DEC NOV AUG MAR Adult longevity (days) and Distance from watercourse (km) and Distance from watercourse (days) Adult longevity

Fig. 5. Mean distance (km) from the main watercourses of veterinary clinics reporting Old World screwworm fly (OWS) cases in 1996–1997 (left-hand axis, solid squares) and adult OWS longevity in 1998–1999 (number of days, left-hand axis, solid circles), plotted with average monthly air temperatures for Central Iraq for 1996–1997 (right-hand axis, triangles) and for 1998–1999 (right hand axis, inverted triangles). at an exponential rate in seasonally favourable conditions At the perimeter of the intercontinental OWS distribution, to give rise to major outbreaks of traumatic myiasis seasonality becomes a natural feature of OWS epidemiology, (Fig. 1). Such epidemics could arise when a number of as it was for NWS in North America. Screwworm critical conditions are met for population multiplication population expansion and regression, in time and space, and dispersal because screwworm fits the pattern of a would appear an innate characteristic of screwworm ecol- ‘boom and bust’ r-strategist (Southwood et al., 1974). ogy and behaviour. For screwworm flies to survive, it is Given the high mobility of the fly and the extensive critically important that a sufficient number of oviposition movement of livestock across the Middle East, occasional sites are encountered (Krafsur & Hightower, 1979; Atzeni major flare-ups are likely to continue in the absence of a et al., 1994). Yet suitable wounds to serve as oviposition sustained international control effort. Remote sensing sites may be a relatively rare resource, favouring widespread and GIS tools may be applied by veterinary and medical dispersal (Spradbery et al., 1995). Given that screwworm services to assist early detection and early response to existed long before the domestication of farm animals, it OWS incursions and flare-ups, as shown by Rogers follows that its ecological features and behaviour go back to (1998) and Hay et al. (1996). the time that wild ungulate hosts prevailed as the main source of wounds for oviposition (Hall et al., 2001). At 7000 that time, and in the absence of today’s ruminant livestock biomass, screwworm flies depended on their ability to cover 6000 large areas and be present in fresh wounds, navels of the 5000 newborn and also other undamaged body orifices in wild- life. Spradbery et al. (1995), in a study carried out during the 4000 south-east Asian (dry) season when conditions were likely 3000 to be hostile for OWS, found a typical dispersal range of 10.8 km for female screwworm flies before depositing an egg 2000 mass. In North America, over several generations C. homi-

Number of OWS cases Number of OWS nivorax populations were found to disperse northwards up 1000 to 2400 km each year, from over-wintering areas in the 0 southern states of the United States and from Mexico, Sparse Light Medium High with an average weekly dispersal of 50–60 km (Barrett, Vegetation density index 1937). As indicated by the results of the present study, Fig. 6. The frequency distribution of Old World screwworm fly adult OWS survival and distribution become severely cur- (OWS) cases according to a satellite-derived vegetation index class; tailed in the field by hot/dry conditions. Seasonality shown for the period of population expansion, September 1996 to becomes a prominent feature at the perimeter of a species January 1997 (grey columns), and for the summer refugia, as distribution, simply because marginal conditions imply indicated by the July to August 1997 foci (black columns). reduced and more variable survival rates. Screwworm

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150 Old World screwworm in Iraq 149 spread requires that the right conditions be met in the Chrysomya bezziana Villeneuve, (Diptera: Calliphoridae). MSc right place, at the right moment and in the right sequence. Thesis, College of Education for Women, University of Multiplication and subsequent fly-dispersal phases become Baghdad, Baghdad (In Arabic). synchronized with seasonal cycles in the environment. In Al-Taweel, A.A., Al-Izzi, M.A.J. & Jassim, F.A. (2000) Incidence situations where there is a wet/cool season followed by a of Old World screw-worm fly, Chrysomya bezziana, in Iraq. Area-Wide Control of Fruit Flies and Other Insect Pests (ed. by hot/dry one there is bound to be a period, even short, K. H. Tan), pp. 101–106. Penerbit Universiti Sains Malaysia, during which pupal development conditions are favourable. Penang. For population expansion, it is critical that this phase be Ansari, M.A. & Oertley, R.E. (1982) Nasal myiasis due to Bezzi’s followed by a period during which conditions are conducive blowfly (screw worm): case report. Saudi Medical Journal, 3, to fly survival and population spread. In Iraq, pupal devel- 275–278. opment conditions are optimal during the spring, but any Atzeni, M.G., Mayer, D.G., Spradbery, J.P., Anaman, K.A. adults that emerge are subjected to the harsh summer con- & Butler, D.G. (1994) Comparison of the predicted impact of ditions (hot and dry) that follow, when adult fly longevity is a screwworm fly outbreak in Australia using a growth index drastically reduced. Hence, conditions for successful OWS model and a life-cycle model. Medical and Veterinary Entomol- introduction are met only during late summer and early ogy, 8, 281–291. Barrett, W.L. (1937) Natural dispersion of Cochliomyia americana. autumn. Journal of Economic Entomology, 30, 873–876. El-Azazy, O.M.E. & El-Metenawy, T.M. (2004) Cutaneous myiasis in Saudi Arabia. Veterinary Record, 154, 305–306. Acknowledgements FAO (1992) The New World Screwworm Eradication Programme, North Africa, pp. 1998–92. FAO Publications, Rome. We are grateful to the International Atomic Energy Agency FAOSTAT (2001) The State of Food and Agriculture, 2001. FAO (IAEA) for provision of supplies towards construction of Publications, Rome. the OWS rearing facility at Tuwaitha. We are also grateful Gabaj, M.M., Wyatt, N.P., Pont, A.C., Beesley, W.N., Awan, to Hassan Partow (UNEP Geneva) for his kind help by M.A.Q., Gusbi, A.M. & Benhaj, K.M. (1989) The Screwworm providing the satellite imageries of the Mesopotamia valley fly in Libya: threat to the livestock industry of the Old World. marshland. The technical support from the SDNR staff at Veterinary Record, 125, 347–349. Groten, S.M.E. (1993) NDVI-crop monitoring and early yield FAO is highly appreciated. 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